Ornis Hungarica 2014. 22(1): 1–14. DOI: 10.2478/orhu-2014-0007 A case study on the phylogeny and conservation of Saker

Krisztián Pomichal1*, Balázs Vági2 & Tibor Csörgő1

Krisztián Pomichal, Balázs Vági & Tibor Csörgő 2014. A case study on the phylogeny and conser- vation of . – Ornis Hungarica 22(1): 1–14.

Abstract The Saker Falcon is a falconid raptor with Palearctic distribution. It has ne­ ver been a common in , now there are cc. 220–230 nesting pairs within the count­ ry borders. Currently total world population is cc. 19 000–34 000 individuals. Its taxonomic status is complica­ ted. Two are distinguished (Falco c. cherrug and Falco c. milvipes); however, molecular data does not support this split. Phylogeny of the species is also not clarified, similarly to closely related raptors. There are ma- ny factors threatening the population of the Saker. One of these factors is the occurrence of the . By molecular investigations more data can be gained, that could be useful in practical conservation, too.

Keywords: Falco cherrug, , , hybridization, conservation

Összefoglalás A kerecsensólyom a sólyomfélék családjába tartozó, palearktikus elterjedésű faj. Magyarországon sosem volt gyakori madár, jelenleg 220–230 pár fészkelhet az országban. A világállomány körülbelül 19 000– 34 000 párt tesz ki. A faj taxonómiája nagyon összetett. Jelenleg két alfaját különböztetik meg, molekuláris bizo- nyítékok azonban nem támasztják alá ezt a felosztást. A faj leszármazási vonala szintén nem tisztázott, ugyanúgy, ahogy a legközelebbi rokon fajoké sem. Számos tényező veszélyezteti a faj állományait, ezek közül az egyik leg- fenyegetőbb a hibrid madarak problematikája. A molekuláris vizsgálatok segítségével olyan ismeretek szerezhe- tőek, melyek haszonnal alkalmazhatóak a gyakorlati természetvédelemben is.

Kulcsszavak: Falco cherrug, filogenetika, taxonómia, hibridizáció, természetvédelem

1 Department of , Cell- and Developmental Biology, Eötvös Loránd University, 1117 , Pázmány Péter sétány 1/c, Hungary, e-mail: [email protected] 2 MTA-ATK-NÖVI Lendület Evolutionary Research Group, 1022 Budapest, Herman Ottó út 15., Hungary *corresponding author

Molecular approaches have been gaining in- e.g. previously undivided world populations creasing importance in every field of biolo- could be split into two or more species. This gy in the last 60 years since the description­ could change conservation categories when of the molecular structure of the DNA. Inves- marginal or isolated subpopulations which tigations on nuclear and mitochondrial ge- comprise only a fraction of the world popu- nomes yielded significant knowledge in seve­­ lation turn out to be separate species. ral streams of biology, which questioned the Certain species may have evolved by hyb­ re le­ vance­ of traditional taxonomic categories ridization and this could be important not and this way affected other research fields as only on a theoretical base but it could have well, e.g. practical nature conservation. practical implications as well. In practice of On one hand, clarifying taxonomic sta- the last decades new hybrids of greater size, tus and relations of recent species could be robustness and superior hunting skills have fascinating, on the other hand new results been created between falconid species. It may challenge widely accepted taxonomy, is dubious whether these hybrids escaping 2 ORNIS HUNGARICA 2014. 22(1) to the wild can reproduce with wild speci- of this was that time common nest looting mens; whether they are capable of creating which concerned mainly nests built on cliffs. viable offspring, and if so how they affect In several cases nesting failure­ was caused the gene pool of wild populations. by human disturbance, and in certain occa- It is also problematic that there is diffe­ sion illegal shooting also happened. The spe- rent legislation affecting trade in hybrids cies has been preserved due to enormous ef- originating from breeding stocks. This po­ forts of nature conservation experts. In 22 ses a threat that captured wild specimens years the population grew from 8 breeding can be traded as hybrids to thwart regula- pairs to 113–145 pairs (Bagyura et al. 2004). tions. Here, we present a case study of such According to latest reports the Hungarian problematic on the Saker Falcon. populations can be estimated 220–230 pairs (Bagyura et al. 2012).

Distribution and population size Taxonomy of the Saker Falcon The Saker Falcon (Falco cherrug Gray, 1834) is a palearctic species belonging to The Saker Falcon was described by the Bri­ the falconid family (). The wes­ tish zoologist John Edward Gray in Hard- tern border of its distribution area is in Cent­ wicke’s book Illustrations of Indian Zoo­ ral Europe, while its eastern border is near logy in 1834. The description was made on the Amur River (Ragyov et al. 2010). The a young raptor wintering in . As resear­ total area of its nesting range and habitats is chers were not aware of its complete distri- cc. 10 300 square kilometres (BirdLife In- bution area, the Saker was described inde- ternational 2012). The world population of pendently by several taxonomists, thus, its the species is decreasing in its whole range, nomenclature has been confused (Ragyov­ et the loss was 32% according to 1991–2010 al. 2009). Previously, six subspecies of the estimation means (the exact value should questionable species were described as fol- be somewhere between 30 and 49 per- lows: F. c. cyanopus (distributed in Central cent). Currently total world population of Europe and along the Volga river), F. c. cher- the species is cc. 19 200–34 000 individu- rug (Russia), F. c. hendersoni (Pamir Moun- als (BirdLife International 2012), but there tains, Himalaya), F. c. altaicus (Altai-Sayan are also world population size estimates Region), F. c. milvipes ( and of 7200–8520 individuals from the year of ), F. c. coatsi (from to Tian 2003 (Bagyura et al. 2007). Shan) (Nittinger et al. 2007). Some authors’ Saker Falcon has never been a common work (e.g. Pfeffer 2009) also mention the Si- bird in Hungary; but in the 1970s its po­ berian Saker (Falco c. saceroides) and the pulation reached a critical state. At the begin- Anatolian Saker­ (F. c. anatolicus). Falco ch. ning of the following decade only 8 breeding saceroides is known as hybrid between the attempts were recorded in the 13 known ter- and the Saker, while F. c. anatoli- ritories. Two of them were successful with cus is an other subspecies. 2-2 fledged juveniles. In 1980 the population­ Most debated is the population of Central on country level have not been more than 30 Asian mountains (Altai, Tian Shan) which is pairs (Bagyura et al. 2004). The main cause considered to be a separate species (the Al- K. Pomichal, B. Vági & T. Csörgő 3 tai Falcon – Falco altaicus) (Moseikin & El- Phylogenetics lis 2004). Others claim that the Altai Falcon is a persistent hybrid­ between the Gyrfalcon The first molecular investigations from the and the Saker Falcon. Based on genetic re- 1960s to the middle of the 1980s were based search the Altai Falcon cannot be separated on allozyme variance. Allozymes are dif- from the other two subspecies of the Saker ferent variants of enzymes which are co­ (Wink et al. 2004). ded at the same locus of the chromosomes. The Saker Falcon is a polytypic species While researchers managed to get informa- with two accepted subspecies: F. c. cherrug tion by direct inspection of the DNA this and F. c. milvipes (Clements et al. 2011). method lost its significance; it has been out- While F. c. cherrug is distributed in Europe competed by DNA sequencing with restric- as well as east from the Yenisei River and tion enzymes and later direct sequencing of the Altai Mountains to , F. c. milvipes the DNA. Recently the whole genome of the is restricted to the northern and eastern parts Saker Falcon has been sequenced. of and North-Eastern China Certain sources treat the Hierofalco group (Ferguson-Lees & Christie 2001). This se­ as a subgenus (Wink & Seibold 1996), paration is based on phenotypic traits solely. while others consider it only as collective Molecular investigations based on micro- terminus without any taxonomic relevance satellites and mitochondrial control regions (Nittinger et al. 2007). Recent species of of DNA samples extracted from skin and the Hierofalco group originate from Afri- plumage of museum specimens failed to de- ca and they spread out of that continent in tect any differences between ssp. cherrug several consecutive waves. This group con- and ssp. milvipes (Nittinger et al. 2007). sists of four species: the Saker Falcon, the Taxonomy of the species is still concer­ Gyrfalcon (F. rusticolus), the Laggar Fal- ning researchers. Some taxonomists claim con (F. jugger) and the (F. that division into two subspecies is over- biarmicus) (Nittinger et al. 2007). Based on simplified (Karyakin 2009, Pfander 2011). some research the (F. subni- Pfeffer (2009) propose a separation of fur- ger) from Australia is also belonging to this ther six subspecies, one of which (F. c. ana- group (Wink et al. 2004). tolicus) has been still undescribed. This The northern and southern populations concept is based on the species’ undoubted- had been separated from each other by the ly remarkable phenotypic variance, which formation and expansion of the Sahara De- is underpinned by the authors’ observa- sert. Northern populations begun to spread tions by traditional methods in nature and towards the Mediterranean area and colo- captivity; however, it contradicts current nized the whole Eurasian continent in three phylogenetic­ results (which are otherwise waves during the warmer periods of the cited in that paper). Pleistocene. The evolved Pfander (2011) suggests the introduction from population spreading towards India of a currently unused taxonomic concept, through the eastern part of the Mediterrane- the ‘semispecies’ to the taxonomy of the an Basin, while the Gyrfalcon evolved from Saker Falcon. He considers that Saker Fal- individuals colonizing the Paleartic. The con is geographically separated and propo­ Saker Falcon came from the Eastern Afri- ses four different semispecies. can coast then evolved in Central Asia. At 4 ORNIS HUNGARICA 2014. 22(1) the end of the both the samples from Hungary as well as Kazakh- Saker and the Gyrfalcon expanded their area stan, but neither clade I nor II corresponded towards north and east respectively, and as to a subspecies or a part of the distribution a consequence a new contact zone formed area (Wink et al. 2004). somewhere in Central Asia, where the two What causes this high level of morpho- species could hybridise with each other. The logical and genetic diversity? The resear­ most ancient species of the group is presu­ chers hypothesize that the above mentioned mably the Lanner Falcon what is supported clades are the results of hybridization events by fossil records. The oldest Hierofalco fos- which happened 100 000–200 000 years sil was discovered in Corsica. It is more than ago between the Saker and the Gyrfalcon 34 000 years old and has been identified as or rather the Lanner Falcon. Considerable­ F. biarmicus (Bonifay et al. 1998, Nittinger vari ­ation observed in the plumage of the Sa­ et al. 2005). However, African fossils of this ker Falcon and the fact that that Saker and species are currently undiscovered. Gyrfalcon can readily hybridise in captivi- Nittinger et al. (2005) performed research ty gives reasonable proof to this argument on 56 DNA samples from the Hierofal- (Wink et al. 2004). co group, all of them originating from wild A more recent study based on mitochond­ with only one exception. They identi- rial control region classified the haplotypes fied 31 haplotypes based on mitochondrial­ into two major groups (A, B) within the control and pseudocontrol regions. They Saker’s population. Altogether 186 indivi­ found that none of the species of the Hi- duals were investigated from the whole dis- erofalco group were monophyletic. Mem- tribution range of the species. In Central bers of the group are closely related to each Europe and in Northern hap- other and separated during the last 1 million lotype group B was the dominant, while in years, what is underpinned by the similarity­ the popu­lations of Central-Asia and Sou­ of haplotypes, confirming the results of pre- thern Siberia haplotype group A was more vious investigations based on cyt-b genes widespread. In Mongolia the frequencies of (e.g. Wink et al. 2004). The observed pat- the two haplotype groups were around the tern of haplotypes could be caused by two, same. Interestingly, only haplotype group A not necessarily contradicting phenomenon:­ was found within the Gyrfalcon population (1) incomplete lineage sorting of ancestral (Nittinger et al. 2007). polymorphism and (2) interspecific gene The authors presume that the ancient po­ flow through hybridization (Nittinger et al. pulation of the Saker Falcon contained only 2005). haplotypes B, while the A haplotypes con- The Saker Falcon proved to be the most quered the genom of the species by intro- diverse species of the Hierofalco group by gression. The introgresson was asymmet- a genetic research on approximately 200 ric, as no Gyrfalcon carrying haplotypes samp ­les covering the whole distribution group B have been found until now. How- area. It can be divided into at least three, ever, we should not draw any conclusions as well-defined clades which were signed with the Gyrfalcon was represented in the study Roman numerals (I, II, III) in the study. All with a low sample size (n=19), although the clades comprise individuals of both recently samp ­les covered the whole distribution area accepted subspecies, e.g. clade III contained of the species (Nittinger et al. 2007). How K. Pomichal, B. Vági & T. Csörgő 5 could this zonality formed between haplo- biguously separate the two species based on groups? The Saker Falcon carrying mitochondrial cytochrome-b and control re- haplotype group B was spreading from the gions. They are not even isolated reproduc- west to the north-east during its presump- tively (Eastham & Nichols 2005). The Sa­ tive postglacial expansion. After reaching­ ker and the Gyrfalcon readily reproduce the grasslands of Kazakhstan it spread into with each other in captivity, their hybrids Dzungaria through the mountains of Tian representing a remarkable percent of falcon- Shan and Altai, and then it reached the are­ ry birds in the (Kenward 2009). as what are now Eastern Mongolia and the Both species are listed on CITES, however, northern regions of China. In the eleva­ their phylogenetic relationships are unex- ted regions of Kazakhstan and Mongolia it plained. Their distinction based on pheno- could have merged with populations of the typic traits is sometimes doubtful, however, Gyrfalcon which carried haplotypes group distinction could be refined with the use of A. These hybrid birds might have been fit- morphometrical characteristics (e.g. wing, ted better to the climatic conditions of these tail and tarsus length) (Eastham & Nichols elevated steppe habitats and thus they sur- 2005). In general, this separation based on vived. Haplotypes A might have been in- genetic markers would yield several bene­­ troduced from here to the areas which are fits. On one hand it would make it possible now called Tibet and Iran. Data gained from to track the origins of illegally captured or mitochondrial DNA is not sufficient to un- poached specimens, and on the other hand doubtedly clarify the origin of haplotype it would help increasing the efficacy of the distribution patterns within the Hierofalco preservation of small, isolated units of the group. This pattern was shaped by several two species (Moritz 1994a). evolutionary processes (hybridization, in- In the study of Dawnay et al. (2008) gene complete lineage sorting) together (Nittin­ of mitochondrial cytochrome oxidase 1 ger et al. 2007). (COI) and nine intranuclear microsatellite To explore phylogenetic relations con- marker of the two species were compared. served mitochondrial and intranuclear The researchers aimed to refine phylogene­ marker genes are sequenced. Among the tic relations between the two species, more- most commonly studied mitochondrial over they wanted to explore if these DNA genes we can find the cytochrome-b (cyt-b), sequences would be suitable for undoubtful the NADH-dehydrogenase 2 (ND2) and the identification of the species. Samples origi- cytochrome oxidase c subunit 1 (COI), with nated from two Gyrfalcon populations (al- which the mitochondrial phylogenetic line­ together 39 samples from one captive and age or haplotype could be reconstructed one wild population) and three Saker popu­­ (Ballard & Rand 2005). If the studied spe- lations (altogether 37 samples, one of the cies has populations with a low level of in- populations was captive). COI region of the ter-population gene flow even the place of DNA is substantially different even among origin can be detected by investigating hap- closely related species, thus it is capable for lotypes of a captured migrating specimen correct species identification (Hebert et al. (Wink 2006). 2004). According to the COI sequences the Former molecular studies (Wink et al. two species are in a paraphyletic relation- 2004, Nittinger et al. 2005) failed to unam- ship. Paraphyletic relations are common on 6 ORNIS HUNGARICA 2014. 22(1) phylogenetic trees of bird species based on rial genes are evolving as a single linkage mitochondrial sequences (Funk & Omland unit. Thus, there is no effect of studying se­ 2003). This could imply that species could veral genes from the mitochondrial genome, not be identified properly. Moreover their as the resulting gene trees will be the same, application can lead to the construction of which would infer false conclusions. Mater- incorrect phylogeny. However, McKay and nal inheritance of the mitochondrial genome Zink (2010) states that the presumptive is also necessary to take into consideration, para ­phyly is often caused by the inherently­ as if a sex-dependent dispersion event hap- flawed taxonomy. Incomplete lineage sor­ pened in the past, the result should be mis- ting resulted from speciation events in the leading (Zink & Barrowclough 2008). Most recent past could also lead to . The migra ­ting bird species of the Palearctic, e.g. authors predict that phylogenetic relation- the Saker Falcon, colonized its recent nest- ships between species can be reconstruct- ing area after the last glacial. In that case ed based on mtDNA, but considering the li­ seve ­ral marker gene sequences can be so mits of this method these sequences could similar between different populations that be also used for distinction between species their investigation would not enable proper­ (McKay & Zink 2010). The most effective diffe­rentiation between them (Waits et al. would be if researchers first explored phylo- 2003, Lovette et al. 2004). geographic patterns by mitochondrial genes Results of Dawnay et al. (2008) streng­ from a large sample size covering the whole then the phylogeny established earlier by distribution area, and then fine-tuned their comparing other mitochondrial regions (e.g. results using nuclear genes and particular- Nittinger et al. 2005). However, the authors ly, Z-linked loci. The authors claim that in state that unambiguous distinction is on- species with a wide distribution mitochond­ ly possible using intranuclear microsatellite rial loci are also suitable for constricting markers. Using this method, individuals of phylogenetic trees (Drovetski et al. 2014). the Gyrfalcon and the Saker could be told However, phylogenetic and phylogeogra­ apart with 98% accuracy. According to the phic results based on mitochondrial DNA authors (Nittinger et al. 2005), the observed have always received criticism. Applica- allelic differences are caused by recent se­ tion of mtDNA has been questioned by pa ­ration of the species and not geographic­ several, claiming that these results are not distance between populations. As a conse- relevant in ecological and conservational re- quence, the method should give reliable­ search. Bazin et al. (2006) were led to this results with a substantially larger sample conclusion by investigating frequently used size, and it was proposed a route use during mtDNA markers from cc. 3000 various ver- CITES controls (Dawnay et al. 2008). tebrate and invertebrate species. They ex- Some researchers aim to explore taxono- plain mtDNA variations found in closely my and ancestry of the species with other related species or populations within a spe- than genetic methods. Karyakin (2011) se­ cies by recurrent adaptive . How- pa ­rated three groups (one western Sa­ ever, they found that intranuclear markers ker and two eastern Sakers) based on spa- are eligible­ for phylogenetic reconstructions tial analysis of eight phenotypic traits, and (Bazin et al. 2006). The main point of criti­­ these groups were further subdivided into cal arguments, however, is that mitochond­ five geographically­ distinct subspecies. This K. Pomichal, B. Vági & T. Csörgő 7 analysis was made on the following traits: respond for Falco c. milvipes and Falco variations of pale pattern of upper body c. cherrug as well), furthermore the recent without wings and tail, colouring of crown, Laggar Falcon could have been isolated this moustache, colouring of upper body, pre­ way. The author considers feasible that the sence and intensity of a bluish-gray shade eastern population of the Saker hybridised and degree of its distribution, colouring of with the western Saker and ‘cap- breast and belly, dark pattern of underbody tured’ in high mountains, which resulted and pale pattern of tail, respectively. Kar- in several hybrid populations. The former yakin (2011) used not only museum speci- could have been a rare hybridization event mens or trapped individuals, but also took due to geographic barriers, while the latter photographs in order to get more compre- could have been a more frequent event, due hensive view of phenotypical variances to the gradual disappearance of those barri- within the population. ers (Karyakin 2011). It is also worth men- Further, Karyakin (2011) drew a more de- tioning that some authors propose a distinc- tailed picture on the phylogenetic relation- tion between ‘eastern’ and ‘western’ form ships of the species within the Hierofalco of the Sakers based upon exactly these as- group. He based his assumptions on a study sumptions (Karyakin 2011, Pfeffer 2012). which states that there were no geographic­ The Saker, the Gyrfalcon and the Laggar isolation between recent area of the Saker Falcon hybridize with each other in capti­ and Gyrfalcon during the middle and late vity. Thus, they can only be considered Pleistocene (Potapov & Sale 2005). This when geography is taken into account. The area was populated by a hypothetic Proto- protofalcon is still separating into four dis- falco species. The geographic barrier, i.e. tinct forms. In woody steppes the ‘western’ the taiga belt, started to form 9–11 thousand Saker’s, while in arid mountains the ‘eas­ years ago, and it increasingly divided nest- tern’ Saker’s speciation is happening now. ing area of the species from the East to the In the mountains of Central Asia hybrids­ of West. However, it is hard to define any geo- the ‘captured’ Gyrfalcons and Sakers­ are graphical barriers in case of excellent flying evolving slowly into a new species, and the species like birds. fourth protofalcon descendants­ are the Gyr- It is worth mentioning that this isolation falcon populations living in the tundra­ belt. was completed faster at the western part of Divergence of the ‘eastern’ Saker is ob­ Eurasia, thus, a corridor remained in the vious, but the western population seems to East, through which gene flow could be be a lot more homogeneous, in which plum- maintained between the populations (Kar- age differences are negligible­ even between yakin 2011). The absolute isolation then populations in far corners of its area. Al- comple ted­ around 6000 years ago. This iso- though gene flow/transfer/exchange could lation resulted in the evolution of at least be implied among these populations,­ but five great falcon species (or subspecies). Of it must have been ceased with the elimina- the two Gyrfalcon populations one evolved tion of populations in the West of the Ural at the extremely fragmented tundra, while Mountains. And it has a very little chance the other one evolved in the high mountains that vagrant young, western­ birds could of Central Asia. Two Saker populations, an hyb ridise­ with Asian specimens (Karyakin­ eastern and a western one (these can cor- 2011). 8 ORNIS HUNGARICA 2014. 22(1)

Hybridization ise with each other, and the hybrids (sup- posedly) preserve their reproductive po- Hybridization among falcon species is rare tential several generation down. According in nature; however, there exist some obser- to Fox (1999) offspring of Hierofalco indi- vations. A male (Falco pe- viduals crossed with Peregrine Falcons are regrinus) and a female (Falco rarely capable to sire, females are often ste­ mexicanus) had a successful breeding in Ca- rile. Contrary, nestings of a Peregrine × Sa­ nada (Oliphant 1991), while in China a nes- ker male and a Saker female were observed ting of a Saker and a (Fal- in several years; eggs were usually sterile co peregrinoides) was observed (Angelov et but their offspring hatched successfully e.g. al. 2006). In Bulgaria several nesting of Sa- in 1999 or in 2003 (BirdLife International ker and Lanner Falcon mixed pairs were do- 2008). cumented (Boev & Dimitrov 1995). In 2005 However, it should not be forgotten that a hatching of female Peregrine Falcon and a birds can hybridise even under natural condi- ‘tribrid’ (Gyrfalcon/Saker × Peregrine) male tion, so it does not necessarily mean an anth- falcon were noted. The pair was reared at ropogenic, often disadvantageous effect, ra­ least two chicks, but the offspring died be- ther an important evolutionary mechanism, fore leaving the nest due to a rock slide and which takes part in the evolution of individu- the hybrid individual was shot (Everitt & al species (Pierotti & Annett 1993, Easthem Franklin 2009). & Nichols 2005). Hybridization is more fre- As keeping captive bred birds spread in quent in bird families and subfamilies where , so spread the crossing between­ males take a large part in raising up offspring, different species. One of the first hybrid and it is much rarer where males invest only clutches was a brood between a female their genetic material into the young. Also re- Saker and a male Peregrine Falcon at the markable is the phenomenon that there is also beginning of the 1970s in Ireland. At first a difference in the number of subspecies. In the crossing was viewed as a pure novel- those bird families where males’ attendance ty, and then it aimed to create new hunting is significant, there are usually more polyty- types for different game species (Kenward pic species. That implies that reproductive 2009). For instance in the Middle East Sa­ isolation may be rare while local adaptations ker was crossed with the Gyrfalcon to uni- are more common. fy Saker‘s speed with the robust physique In the Falconidae family intergeneric hyb­ of the Gyrfalcon (Kenward 2009). These ridization was observed in seven out of 57 specimens are also more tolerant to heat species (Pierotti & Annett 1993). and diseases (Fox 1999). Recent hybridization could be excluded­ Divergence between the Saker, the Gyr- between allopatric species pairs: F. rusti- falcon and the Lanner Falcon is very small, colus/F. jugger and F. biarmicus/F. rusti- the interspecific genetic distance is only colus, but not between Saker, Lanner and 0.4–2.0%. Interestingly, taxa with a similar Laggar Falcons. There are potential hybrid degree of relatedness are considered sub- zones in and India (in south-wes­ species in several other genera (Wink et al. tern nesting areas of the Laggar Falcon), 2004). It is not surprising thus that species further in the Balkan Peninsula and Ana- of the Hierofalco group are easily hybrid- tolia (nesting areas of the northern popula- K. Pomichal, B. Vági & T. Csörgő 9 tions of the Lanner Falcon). Certain speci- ted Kingdom neither hybrid specimens will mens of the Lanner and the Laggar Falcon need a registration in the future according­ to get in contact in Southern Iran and Pakis­ recent plans (BirdLife International 2008). tan, while the Saker can get in touch with It poses serious conservational concerns as the Gyrfalcon in Southern Siberia during the more than 4000 out of 8000 falcon speci- nesting season (Moseikin & Ellis 2004, Nit- mens kept in captivity in the country are tinger et al. 2007). hybrid birds, whilst the majority of them In Europe every year several hundreds of (44%) are hybrids of Sakers and Gyrfalcons hybrid falcons escape from their owner­ or (Fleming et al. 2011). released into the wild. In the Middle East frequency of such events are estimated to an order of several thousand each spring Applying taxonomic results in (Lindberg 2006). In Great Britain more practice than 1500 Peregrine Falcons escaped from captivity between 1983 and 2007, around Conservation biology can take out seve­ 40% of which were hybrid birds (Fleming ral benefits from the results of molecular re- et al. 2011). search. On one hand, it can expand know­ Based on samples from 156 specimens of ledge on the evolution and ecology of species, seven falcon species Nittinger et al. (2006) on the other hand, the acquired knowledge concluded that hybrid birds have a huge im- may be used for solving concrete prob- pact on the gene pool of Saker Falcons li­ lems. By exploring genetic differentiation of ving wild in Europe. According to samples popu lations­ we can recognize those popula- collected between 1970 and 2003, 21% of tions which are genetically the most diffe­ individuals were a hybrids or descendants of rent from massive population blocks. These hybrid birds (Nittinger et al. 2006). Thus in- small population fragments which have the terspecific genetic introgression poses areal greatest genetic variability are the most valu­ threat. able and most threatened (Friesen 2007). BirdLife International promoted a to- Those populations between which there is tal ban on keeping and breeding hybrid fal- no gene exchange, thus which are separated cons, although there is no adequate infor- both demographically and evolutionary, are mation on the negative effects of hybrid called Evolutionary Significant Units (ESU) birds getting to the nature. The organiza- (Moritz 1994b in Friesen 2007). These ESUs tion is arguing that there is no serious rea- are present in several conservational direc- son for breeding hybrid birds, as such speci- tives (e.g. US Act). mens are unsuitable for ex situ conservation For applying appropriate conservation programmes, whilst banning would cause programmes and directives, correct taxono­ disadvantage for only a fistful of economic­ my of the focal species should be known. stakeholder. In six countries of the Europe- For instance, protection of the ‘Altai’ Fal- an Union (including Hungary) falconry use con would call for different legislation if it of hybrid birds has been already banned. was considered a separate species, or on- However, in several other countries even ly a colour­ variant of the Saker. Regar­ the ringing and registration of hybrid rap- ding as a separate species may have a fur- tors is not mandatory, moreover in the Uni­ ther advantage for the Altai Falcon, namely 10 ORNIS HUNGARICA 2014. 22(1) it draws attention to the Central Asian popu­ rate identification would require genetic in- lation, inspiring further research on it (Fer- vestigations. guson-Lees & Christie 2001). An adequate solution would be the intro- Hybridization has a particular importance duction of a registration system, although from the viewpoint of nature conservation. legislative framework is not available in Hybrid specimens getting into the wild po­ several countries (BirdLife International ses a potential threat to natural populations 2008). Thus there is the possibility that il- of the species as hybrids may deteriorate legally captured pure breed individuals can gene pool. Several cases of nestings between be sold as hybrids. Apart from the threat of escaped or released and wild birds have been genetic introgression discussed above a fur- documented (Fox 1999, Kleinstauber & See- ther problem may arise when escaped or re- ber 2000). Genetic research also attributes a leased hybrids circumvent nesting of wild remarkable effect to hybrid species (Nittin­ birds, as it was observed in the case of Pe­ ger et al. 2006). BirdLife International regrine Falcons in the Netherlands (BirdLife (2008) regards these birds as one of the main International 2008). threats to the European Saker population. Hybridization could have direct conserva- Without precise legislation and appropriate tional risk. For example, the greater Spotted implements it is extremely troublesome to (Aquila clanga) is a rare raptor spe- separate young hybrid and full-blood speci- cies of Eastern Europe, which frequently mens; by using phenotypic traits it is almost hybridise in nature with its more common impossible, and even genetic markers not al- relative, the Lesser Spotted Eagle (Aquila ways show a clear picture. pomarina). Researchers studying the gene­ Eastham and Nicholls (2005) studied phe- tics of 14 European Greater Spotted Eagle notypic traits of the Gyrfalcon, the Pereg­ populations found evidence for hybridiza- rine Falcon, the Saker and the New Zealand tion or introgression in all of them. In most Falcon (Falco novaeseelandiae) together­ regions hybrids originating from male Les­ with their hybrids, and also investigated ser Spotted Eagles and female Grater Spot- how this data could be used for the identi- ted Eagles were observed. In those areas fication of hybrid individuals. Allrid hyb­ where Greater Spotted Eagle maintains a specimens were born in captivity, thus their larger population size hybridization was less descent was clear. The researchers found frequent. The Estonian population is par- that phenotypes of the offspring are more ticularly threatened as more Greater Spot- similar to the males’ phenotypes compared ted Eagle females were found paired with a to those of the females. This result is fur- Lesser Spotted Eagle male than with a con- ther strengthened by earlier genetic find- specific partner, thus it can be declared that ings that two third of genes linked to sex hybridization of species could pose a real being carried by the males. This study high- danger for populations of certain protected lights the problem that discerning full-blood species (Väli et al. 2010). speci ­mens from their hybrids is often diffi- BirdLife International (2008) suggests cult (particularly hybrids of the Gyrfalcon the following proposal for mitigation of the and the Saker), and young individuals are problem: especially difficult to discern based on the – Hybrid offspring should be raised by pairs plumage (Eastham & Nicholls 2005). Accu- of species which are not occurring locally K. Pomichal, B. Vági & T. Csörgő 11

– Hybrids can only be hacked in large con- As in other fields of zoology, in ornitholo- ditioning pens gy, the results of molecular taxonomy have – Hybrids should be only let fly with appro- substantially changed systematics built upon priate telemetric devices phenotypic traits. Taxonomy of the New – Every effort should be made to find -es World vultures is a prominent example of caped hybrid birds the essentially conflicting results of the two – Hybrid specimens should never be wilful- approaches (Avise et al. 1994, Wink 1995). ly released under any circumstances Later research based on mitochondrial and Breeders and falconers are on the opinion intranuclear genes questioned the monophy- that crossing species is helping to improve ly of Old World vultures, too (Lerner & Min- birds’ attributes, hence their activity is ad- del 2005). By investigating different markers vantageous and should be supported. How- several groups seemed to be far from each ever, if individual species are treated as other have been finally linked together. Con- sepa ­rate biological unit to be protected, we sequences deduced from the results, how- are regarding things from a different point ever, sometimes fundamentally contradict of view. Crossing species is then harmful for to each other, caused by, for instance, diffe­ their genetic integrity, provoking conserva- rences in the position of the studied gene se- tional concerns. quences within the cell (Bensch et al. 2005, Although breeding of hybrids poses some Brito 2007). Thus, it is important to empha- risks, with an appropriate legislation this size that phylogenetic relationships could be technique may have a leading role in the deduced correctly by considering the results preservation of endangered species (Fox of both classical and molecular taxonomy. 1999). However, it is worth mentioning that the practice of crossing falconry birds is only 40 years old and thus it is difficult to Acknowledgements predict the effects of spreading hybrids on natural populations without any long-term We would like to express our gratitude to re- monitoring. ferees and József Vuts, who made the lan- guage corrections for the paper.

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